Artificial nighttime light changes aphid parasitoid population dynamics 1Scientific RepoRts | 5 15232 | DOi 10 1038/srep15232 www nature com/scientificreports Artificial nighttime light changes aphid[.]
www.nature.com/scientificreports OPEN Artificial nighttime light changes aphid-parasitoid population dynamics received: 17 June 2015 accepted: 09 September 2015 Published: 16 October 2015 Dirk Sanders1, Rachel Kehoe1, Katie Tiley1, Jonathan Bennie2, Dave Cruse2, Thomas W. Davies2, F. J. Frank van Veen1 & Kevin J. Gaston2 Artificial light at night (ALAN) is recognized as a widespread and increasingly important anthropogenic environmental pressure on wild species and their interactions Understanding of how these impacts translate into changes in population dynamics of communities with multiple trophic levels is, however, severely lacking In an outdoor mesocosm experiment we tested the effect of ALAN on the population dynamics of a plant-aphid-parasitoid community with one plant species, three aphid species and their specialist parasitoids The light treatment reduced the abundance of two aphid species by 20% over five generations, most likely as a consequence of bottom-up effects, with reductions in bean plant biomass being observed For the aphid Megoura viciae this effect was reversed under autumn conditions with the light treatment promoting continuous reproduction through asexuals All three parasitoid species were negatively affected by the light treatment, through reduced host numbers and we discuss induced possible behavioural changes These results suggest that, in addition to direct impacts on species behaviour, the impacts of ALAN can cascade through food webs with potentially far reaching effects on the wider ecosystem The introduction of artificial lighting into the nighttime environment arguably constitutes one of the most profound environmental pressures to have been exerted by humans Such lighting derives from a diversity of sources (including street lighting) and has already become widespread1 It is continuing to spread rapidly2, and interacts and synergises with many other environmental pressures3 Artificial light at night (ALAN) constitutes an evolutionarily novel anthropogenic environmental pressure for which there have been no natural analogues3; natural light cycles have remained largely stable for millennia, allowing “light guided” biological responses to become evolutionarily and phylogenetically deep rooted Large numbers of studies have documented the effects of ALAN on organismal physiology and behaviour4 These responses have repeatedly been predicted to impact population dynamics of species5 However, empirical studies, and especially experimental ones, largely remain wanting6,7 Studies of the impacts of ALAN on population dynamics would particularly benefit from (i) using established model systems; (ii) running experiments for multiple generations; (iii) examining multiple trophic levels; and (iv) determining effects on the numbers of organisms that are not simply a consequence of organismal movements into or away from the area that is lit5 Here we report the results of an experimental study of the impacts of ALAN on a multi-species plant-aphid-parasitoid system Plant-aphid-parasitoid systems are used widely as models in ecological research because of their abundance and importance in most temperate terrestrial ecosystems and the tractability of host-parasitoid interactions There are several reasons to predict that such systems will be susceptible to ALAN First, studies have shown that the life cycles of aphids are sensitive to changes in light regime, with the length of the photoperiod an important influence that either increases or decreases fecundity depending on species Centre for Ecology & Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall, TR10 9EZ, United Kingdom 2Environment & Sustainability Institute, University of Exeter, Cornwall Campus Penryn, Cornwall, TR10 9EZ, United Kingdom Correspondence and requests for materials should be addressed to D.S (email: d.sanders@exeter.ac.uk) Scientific Reports | 5:15232 | DOI: 10.1038/srep15232 www.nature.com/scientificreports/ and factors such as light intensity and temperature8 Under spring/summer conditions aphids reproduce asexually but can switch to sexual reproduction in autumn (a strategy preferable under harsh winter conditions), again under the influence of the reduction in length of the daily photoperiod9 Second, it is also known that many flying insects change their behaviour when exposed to ALAN10, and there is evidence that changing the photoperiod also affects fecundity in parasitoids (e.g.11) Third, aphids and their parasitoids are not only common in many temperate habitats, but also on vegetation in urban, agricultural and natural ecosystems exposed to varying amounts of ALAN In an outdoor mesocosm experiment with a nighttime lighting treatment and unlit control we tested for the effect of ALAN on the population dynamics of aphids and associated parasitoids, and on aphid host plant biomass, using a community with one plant species and three aphid species and their specialist parasitoids12,13 We predicted that (1) ALAN would decrease aphid population sizes, as this appeared to be the most likely outcome for temperatures below 20 °C and an extended photoperiod8, and (2) the production of aphid sexuals and the number of eggs laid under autumn conditions would be reduced by increasing the perceived daylength Further, (3) we predicted a negative impact of artificial light on parasitoids by reducing their population size as a consequence of reduced host numbers Results Aphids. Over the course of the experiment (approx aphid generations) total aphid abundance (summing across species) was on average reduced by 20% in the light treatment, an effect that changed over time (treatment x time interaction: L Ratio = 7.25, p = 0 .0071) The dominant aphid M viciae and its parasitoid A megourae showed a remarkably quick response to the light treatment with differences in abundance already visible a few days after the lights were switched on (Fig. 1) The negative effect on M viciae was reversed towards the end of the experiment (time x treatment interaction L ratio = 8.58, p = 0.0034) Light treatment had no effect on numbers of males and egg production in M viciae (Fig. 2, L ratio = 1.36, p = 0.2435 ; L ratio = 1.67, p = 0.1968, respectively) A pisum was also negatively influenced by light treatment (L ratio = 9.55 , p = 0.002) while there was no effect on A fabae (L ratio = 2.06, p = 0.1512) Parasitoids. During the experiment (4 parasitoid generations) overall parasitoid abundance declined by 40% in the light treatment (L Ratio = 4.27, p = 0.0388) A megourae followed the pattern of its host, with a strong negative impact of light treatment in the beginning that was less obvious toward the end (L ratio = 4.56, p = 0.0327, Fig. 1) L fabarum was very strongly affected by light treatment in the first three weeks (L ratio = 7.12, p = 0.0076) despite there being no population response of its host to the treatment A ervi was similarly to the other parasitoid species, but less strongly, affected by artificial light (L ratio = 5.17, p = 0.023) Parasitism rate for L fabarum dropped from 0.8% in the control to 0.4% in the light treatment (Fig. 3, z = –2.81, p = 0.00501), while there was no significant change for A megourae and A ervi (Fig. 3, z = − 0.80, p = 0.42; z = − 0.38, p = 0.70, respectively) Plant biomass. Plant biomass was not affected by aphid abundance After the removal of two outliers (unusual high plant biomass) in the dataset, light treatment reduced mean aboveground plant biomass from 1.46 g (± 0.2 SE) in the control treatment to 0.99 g (± 0.1) per plant pot (L Ratio = 6.78, p = 0.0092) In the follow on experiment testing the impact of artificial light on plants without aphids, plant biomass was similarly reduced from 13.5 g ± 0.4 in the control cages to 11.7 g ± 0.5 in light treatment cages (L Ratio = 7.33, p = 0.0068) Discussion With the exception of work on a microbial and on another insect community6,7, this is, in terms of generations, the longest running experiment on the population effects of ALAN to have been reported to date Strong negative effects of ALAN on abundances were found both for aphids and their parasitoids (Fig. 1) Indeed, for the aphid M viciae and its parasitoid these responses were observed surprisingly quickly (within one week) and sustained until close to the end of the experiment when the impact of the light treatment on population size switched to positive by promoting the continuous production of asexuals The responses of animal populations to ALAN can potentially result from a direct impact (e.g growth rate or production of sexuals) or indirectly through bottom-up (resource controlled), top-down (predator or parasite), or non-trophic (e.g competition) processes7 For the aphid species, declines in numbers as a consequence of ALAN in the experiments reported here most likely arose from bottom-up effects, with reductions in bean plant biomass and plant quality due to light treatment reducing the resource available to these herbivores Low intensity light at night, at levels similar to those used in this study, can alter resource allocation and growth form in plants in complex ways, including suppressing growth14 In a previous study7, bottom-up effects of ALAN on an aphid population were likely driven by supressing flowering in their leguminous foodplant and decreasing the abundance of resources The simultaneous negative effect of the ALAN treatment on parasitoid numbers makes it unlikely that any top-down effect could be operating in this study by an increased attack rate leading to lower aphid numbers For M viciae, populations subjected to ALAN became more abundant relative to the controls towards the end of the experiment (Fig. 1) This is a consequence of the continuous production of asexuals under ALAN, showing that this can alter the normal seasonal strategy of switching to sexual reproduction in Scientific Reports | 5:15232 | DOI: 10.1038/srep15232 www.nature.com/scientificreports/ Figure 1. Population dynamics (means of replicates + standard error) of the aphid species Megoura viciae, Aphis fabae and Acyrthosiphon pisum each attacked by a specialist parasitoid namely Aphidius megourae, Lysiphlebus fabarum and Aphidius ervi, in control (black) and light treatment (grey) cages *p